References

Biogeosciences

1726-4189

Copernicus Publications

Göttingen, Germany

10.5194/bg-5-779-2008

Implications of CO2 pooling on δ13C of ecosystem respiration and leaves in Amazonian forest

de Araújo

A. C.

¹ Ometto

J. P. H. B.

² ⁵ Dolman

A. J.

¹ Kruijt

³ Waterloo

M. J.

¹ Ehleringer

J. R.

⁴

Department of Hydrology and Geo-Environmental Sciences, Faculty of Earth and Life Sciences, Vrije Universiteit, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands

Laboratório de Ecologia Isotópia, Centro de Energia Nuclear na Agricultura, USP, Av. Centenário, 303, Piracicaba, SP, CEP 13416-190, Brazil

Earth System Science-Climate Change, Centre for Water and Climate, Wageningen-UR, PO Box 47, 6700 AA, Wageningen, The Netherlands

Department of Biology, University of Utah, 257S 1400E, Salt Lake City, UT, 84112-0840, USA

IGBP Regional Office/INPE, Av. dos Astronautas, 1.758 - Jd. Granja, São José dos Campos, SP, CEP 12227-010, Brazil

14 05 2008

5 3 779 795

2008

This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/

This article is available from https://bg.copernicus.org/articles/5/779/2008/bg-5-779-2008.html

The full text article is available as a PDF file from https://bg.copernicus.org/articles/5/779/2008/bg-5-779-2008.pdf

The carbon isotope of a leaf (δ13Cleaf) is generally more negative in riparian zones than in areas with low soil moisture content or rainfall input. In Central Amazonia, the small-scale topography is composed of plateaus and valleys, with plateaus generally having a lower soil moisture status than the valley edges in the dry season. Yet in the dry season, the nocturnal accumulation of CO2 is higher in the valleys than on the plateaus. Samples of sunlit leaves and atmospheric air were collected along a topographical gradient in the dry season to test whether the δ13Cleaf of sunlit leaves and the carbon isotope ratio of ecosystem respired CO2 (δ13CReco) may be more negative in the valley than those on the plateau. The δ13Cleaf was significantly more negative in the valley than on the plateau. Factors considered to be driving the observed variability in δ13Cleaf were: leaf nitrogen concentration, leaf mass per unit area (LMA), soil moisture availability, more negative carbon isotope ratio of atmospheric CO2 (δ<sp>13Ca) in the valleys during daytime hours, and leaf discrimination (Δleaf). The observed pattern of δ13Cleaf might suggest that water-use efficiency (WUE) is higher on the plateaus than in the valleys. However, there was no full supporting evidence for this because it remains unclear how much of the difference in δ13Cleaf was driven by physiology or &delta13Ca. The δ13CReco was more negative in the valleys than on the plateaus on some nights, whereas in others it was not. It is likely that lateral drainage of CO2 enriched in 13C from upslope areas might have happened when the nights were less stable. Biotic factors such as soil CO2 efflux (Rsoil) and the responses of plants to environmental variables such as vapor pressure deficit (D) may also play a role. The preferential pooling of CO2 in the low-lying areas of this landscape may confound the interpretation of δ13Cleaf and δ13CReco.

References 1

Araujo, A. C., Nobre, A. D., Kruijt, B., Elbers, J. A., Dallarosa, R., Stefani, P., von Randow, C., Manzi, A. O., Culf, A. D., Gash, J. H. C., Valentini, R., and Kabat, P.: Comparative measurements of carbon dioxide fluxes from two nearby towers in a central Amazonian rainforest: The Manaus LBA site, J. Geophys. Res.-Atmos., 107(D20),8090, https://doi.org/10.1029/2001JD000676, 2002.

Bonal, D., Sabatier, D., Montpied, P., Tremeaux, D., and Guehl, J. M.: Interspecific variability of $\delta ^13$C among trees in rainforests of French Guiana: functional groups and canopy integration, Oecologia, 124, 454–468, 2000.

Bowling, D. R., Cook, C. S., and Ehleringer, J. R.: Technique to measure CO2 mixing ratio in small flasks with a bellows/IRGA system, Agricultural and Forest Meteorology, 109, 61–65, 2001.

Bowling, D. R., McDowell, N. G., Bond, B. J., Law, B. E., and Ehleringer, J. R.: $^13$C content of ecosystem respiration is linked to precipitation and vapor pressure deficit, Oecologia, 131, 113–124, 2002.

Broadmeadow, M. S. J., Griffiths, H., Maxwell, C., and Borland, A. M.: The carbon isotope ratio of plant organic material reflects temporal and spatial variations in CO2 within tropical forest formations in Trinidad, Oecologia, 89, 435–441, 1992.

Buchmann, N., Guehl, J. M., Barigah, T. S., and Ehleringer, J. R.: Interseasonal comparison of CO2 concentrations, isotopic composition, and carbon dynamics in an Amazonian rainforest (French Guiana), Oecologia, 110, 120–131, 1997.

Chambers, J. Q., Tribuzy, E. S., Toledo, L. C., Crispim, B. F., Higuchi, N., dos Santos, J., Araujo, A. C., Kruijt, B., Nobre, A. D., and Trumbore, S. E.: Respiration from a tropical forest ecosystem: partitioning of sources and low carbon use efficiency, Ecological Applications, 14, S72–S88, 2004.

Chauvel, A., Lucas, Y., and Boulet, R.: On the genesis of the soil mantle of the region of Manaus, Central Amazonia, Brazil, Experientia, 43, 234–241, 1987.

Conway, T. J., Lang, P. M. and Masarie, K. A.: Atmospheric carbon dioxide dry air mole fractions from the NOAA ESRL carbon cycle cooperative global air sampling network, 1968–2006, version: 2007-09-19, available at: ftp://ftp.cmdl.noaa.gov/ccg/co2/flask/event/, 2007.

Dawson, T. E., Mambelli, S., Plamboeck, A. H., Templer, P. H., and Tu, K. P.: Stable isotopes in plant ecology, Annual Review of Ecology and Systematics, 33, 507–559, 2002.

de Ara\'ujo, A. C., Kruijt, B., Nobre, A. D., Dolman, A. J., Waterloo, M. J., Moors, E. J., and Souza, J. S.: Nocturnal accumulation of CO2 underneath a tropical forest canopy along a topographical gradient, Ecological Applications, in press, 2008.

Ehleringer, J. R., Field, C. B., Lin, Z. F., and Kuo, C. Y.: Leaf carbon isotope and mineral-composition in subtropical plants along an irradiance cline, Oecologia, 70, 520–526, 1986.

Ehleringer, J. R., Lin, Z. F., Field, C. B., Sun, G. C., and Kuo, C. Y.: Leaf carbon isotope ratios of plants from a subtropical monsoon forest, Oecologia, 72, 109–114, 1987.

Ehleringer, J. R. and Rundel, P. W.: Stable isotopes: History, units, and instrumentation, in: Stable isotopes in ecological research, 1 ed., edited by: Rundel, P. W., Ehleringer, J. R., and Nagy, K. A., Ecological studies, Springer-Verlag, New York, USA, 1–15, 1989.

Ehleringer, J. R. and Cook, C. S.: Carbon and oxygen isotope ratios of ecosystem respiration along an Oregon conifer transect: preliminary observations based on small-flask sampling, Tree Physiology, 18, 513–519, 1998.

Ekblad, A. and Hogberg, P.: Natural abundance of $^13$C in CO2 respired from forest soils reveals speed of link between tree photosynthesis and root respiration, Oecologia, 127, 305–308, 2001.

Farquhar, G. D., Oleary, M. H., and Berry, J. A.: On the relationship between carbon isotope discrimination and the inter-cellular carbon-dioxide concentration in leaves, Australian Journal of Plant Physiology, 9(2), 121–137, 1982.

Farquhar, G. D., Ehleringer, J. R., and Hubick, K. T.: Carbon isotope discrimination and photosynthesis, Annual Review of Plant Physiology and Plant Molecular Biology, 40, 503–537, 1989a.

Farquhar, G. D., Hubick, K. T., Condon, A. G., and Richards, R. A.: Carbon isotope fractionation and plant water-use efficiency, in: Stable isotopes in ecological research, 1 ed., edited by: Rundel, P. W., Ehleringer, J. R., and Nagy, K. A., Ecological studies, Springer-Verlag, New York, USA, 21–39, 1989b.

Ferraz, J., Ohta, S., and Sales, P. C.: Distribuição dos solos ao longo de dois transectos em floresta primária ao norte de Manaus (AM), in: Pesquisas florestais para a consevação da floresta e reabilitação de áreas degradadas da Amazônia, 1st ed., edited by: Higuchi, N., Campos, M. A. A., Sampaio, P. T. B., and dos Santos, J., Espaço Comunicação Ltda., Manaus, Brazil, 264, 1998.

Flanagan, L. B., Kubien, D. S., and Ehleringer, J. R.: Spatial and temporal variation in the carbon and oxygen stable isotope ratio of respired CO2 in a boreal forest ecosystem, Tellus Series B-Chemical and Physical Meteorology, 51, 367–384, 1999.

Friend, A. D., Woodward, F. I., and Switsur, V. R.: Field-measurements of photosynthesis, stomatal conductance, leaf nitrogen and $\delta ^13$C along altitudinal gradients in Scotland, Functional Ecology, 3, 117–122, 1989.

Galvão, M. S.: Dinâmica espacial e sazonal da composição isotópica do CO2 respirado por meio do solo em uma floresta primária na Amazônia Central, M. S. thesis, Departamento de Ciências Florestais Tropicais, Instituto Nacional de Pesquisas da Amazônia, Universidade Federal do Amazonas, Manaus, Brazil, 63 pp., 2005.

Garten, C. T. and Taylor, G. E.: Foliar $\delta ^13$C within a temperature deciduous forest: spatial, temporal, and species sources of variation, Oecologia, 90, 1–7, 1992.

Glover, T. J., and Mitchell, K. J.: An introduction to biostatistics, 1st ed., McGraw-Hill Higher Education, New York, 416 pp., 2002.

Goulden, M. L., Miller, S. D., da Rocha, H. R., Menton, M. C., de Freitas, H. C., Figueira, A., and de Sousa, C. A. D.: Diel and seasonal patterns of tropical forest CO2 exchange, Ecological Applications, 14, S42–S54, 2004.

Goulden, M. L., Miller, S. D., and da Rocha, H. R.: Nocturnal cold air drainage and pooling in a tropical forest, J. Geophys. Res.-Atmos., 111, D08S04, https://doi.org/10.1029/2005JD00637, 2006.

Guehl, J. M., Domenach, A. M., Bereau, M., Barigah, T. S., Casabianca, H., Ferhi, A., and Garbaye, J.: Functional diversity in an Amazonian rainforest of French Guyana: a dual isotope approach ($\delta^15$ N and $\delta ^13$C), Oecologia, 116, 316–330, 1998.

Guillaumet, J. L.: Some structural and floristic aspects of the forest, Experientia, 43, 241–251, 1987.

Hanba, Y. T., Noma, N., and Umeki, K.: Relationship between leaf characteristics, tree sizes and species distribution along a slope in a warm temperate forest, Ecological Research, 15, 393–403, 2000.

Keeling, C. D.: The concentration and isotopic abundances of atmospheric carbon dioxide in rural areas, Geochimica et Cosmochimica Acta, 13, 322–334, 1958.

Keeling, C. D., Bollenbacher, A. F., and Whorf, T. P.: Monthly atmospheric $^13$C/$^12$C isotopic ratios for 10 SIO stations, in: Trends: A compendium of data on global change, Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tenn, USA, available at: http://cdiac.ornl.gov/trends/co2/iso-sio/iso-sio.html, 2005a.

Keeling, C. D., Piper, S. C., Bacastow, R. B., Wahlen, M., Whorf, T. P., Heimann, M., and Meijer, H. A.: Atmospheric CO2 and $^13$CO2 exchange with the terrestrial biosphere and oceans from 1978 to 2000: Observations and carbon cycle implications, in: A history of atmospheric CO2 and its effects on plants, animals, and ecosystems, 1 ed., edited by: Ehleringer, J. R., Cerling, T. E., and Dearing, M. D., Ecological studies, Springer Science+Business Media, Inc., New York, USA, 83–113, 2005b.

Knohl, A., Werner, R. A., Brand, W. A., and Buchmann, N.: Short-term variations in $\delta ^13$C of ecosystem respiration reveals link between assimilation and respiration in a deciduous forest, Oecologia, 142, 70–82, 2005.

Korner, C. and Woodward, F. I.: The dynamics of leaf extension in plants with diverse altitudinal ranges II. Field studies in \textitPoa species between 600 and 3200 m altitude, Oecologia, 72, 279–283, 1987.

Korner, C., Farquhar, G. D., and Roksandic, Z.: A global survey of carbon isotope discrimination in plants from high-altitude, Oecologia, 74, 623–632, 1988.

Korner, C., Farquhar, G. D., and Wong, S. C.: Carbon isotope discrimination by plants follows latitudinal and altitudinal trends, Oecologia, 88, 30–40, 1991.

Lai, C. T., Ehleringer, J. R., Tans, P., Wofsy, S. C., Urbanski, S. P., and Hollinger, D. Y.: Estimating photosynthetic $^13$C discrimination in terrestrial CO2 exchange from canopy to regional scales, Global Biogeochemical Cycles, 18, GB1041, https://doi.org/10.1029/2003GB002148, 2004.

Lai, C. T., Ehleringer, J. R., Schauer, A. J., Tans, P. P., Hollinger, D. Y., Paw U, K. T., Munger, J. W., and Wofsy, S. C.: Canopy-scale $\delta^13$C of photosynthetic and respiratory CO2 fluxes: observations in forest biomes across the United States, Glob. Change Biol., 11, 633–643, 2005.

Lloyd, J., Kruijt, B., Hollinger, D. Y., Grace, J., Francey, R. J., Wong, S. C., Kelliher, F. M., Miranda, A. C., Farquhar, G. D., Gash, J. H. C., Vygodskaya, N. N., Wright, I. R., Miranda, H. S., and Schulze, E. D.: Vegetation effects on the isotopic composition of atmospheric CO2 at local and regional scales: theoretical aspects and a comparison between rain forest in Amazonia and a boreal forest in Siberia, Australian Journal of Plant Physiology, 23, 371–399, 1996.

Luizão, R. C. C., Luizão, F. J., Paiva, R. Q., Monteiro, T. F., Sousa, L. S., and Kruijt, B.: Variation of carbon and nitrogen cycling processes along a topographic gradient in a central Amazonian forest, Glob. Change Biol., 10, 592–600, 2004.

Marshall, J. D., and Zhang, J.: Altitudinal variation in carbon isotope discrimination by conifers, in: Stable isotopes and plant carbon-water relations, 1 ed., edited by: Ehleringer, J. R., Hall, A. E., and Farquhar, G. D., Physiological ecology, Academic Press, Inc., San Diego, USA, 187–200, 1993.

Martinelli, L. A., Almeida, S., Brown, I. F., Moreira, M. Z., Victoria, R. L., Sternberg, L. S. L., Ferreira, C. A. C., and Thomas, W. W.: Stable carbon isotope ratio of tree leaves, boles and fine litter in a tropical forest in Rondônia, Brazil, Oecologia, 114, 170–179, 1998.

McDowell, N. G., Bowling, D. R., Schauer, A., Irvine, J., Bond, B. J., Law, B. E., and Ehleringer, J. R.: Associations between carbon isotope ratios of ecosystem respiration, water availability and canopy conductance, Glob. Change Biol., 10, 1767–1784, 2004.

Medina, E., and Minchin, P.: Stratification of $\delta ^13$C values of leaves in Amazonian rain forests, Oecologia, 45, 377–378, 1980.

Medina, E., Montes, G., Guevas, E., and Rokzandic, Z.: Profiles of CO2 concentration and $\delta ^13$C values in tropical rain forests of the upper Rio Negro Basin, Venezuela, Journal of Tropical Ecology, 2, 207–217, 1986.

Medina, E., Sternberg, L., and Cuevas, E.: Vertical stratification of $\delta^13$C values in closed natural and plantation forests in the Luquillo mountains, Puerto Rico, Oecologia, 87, 369–372, 1991.

Mortazavi, B., Chanton, J. P., Prater, J. L., Oishi, A. C., Oren, R., and Katul, G.: Temporal variability in $^13$C of respired CO2 in a pine and a hardwood forest subject to similar climatic conditions, Oecologia, 142, 57–69, 2005.

Nardoto, G. B.: Abundância natural de $^15$N na Amazônia e Cerrado - implicações para ciclagem de nitrogênio, Ph.D thesis, Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, Piracicaba, 100 pp., 2005.

Oliveira, A. A. de and Mori, S. A.: A central Amazonian terra firme forest. I. High tree species richness on poor soils, Biodiversity and Conservation, 8, 1219–1244, 1999.

Oliveira, A. N. de, and Amaral, I. L. d.: Florística e fitossociologia de uma floresta de vertente na Amazônia Central, Amazonas, Brasil, Acta Amazonica, 34, 21–34, 2004.

Oliveira, A. A. de, and Amaral, I. L. d.: Aspectos florísticos, fitossociológicos e ecológicos de um sub-bosque de terra firme na Amazônia Central, Amazonas, Brasil, Acta Amazonica, 35, 1–16, 2005.

Ometto, J. P. H. B., Flanagan, L. B., Martinelli, L. A., Moreira, M. Z., Higuchi, N., and Ehleringer, J. R.: Carbon isotope discrimination in forest and pasture ecosystems of the Amazon Basin, Brazil, Glob. Biogeochem. Cy., 16(4), 1109, https://doi.org/10.1029/2001gb001462, 2002.

Ometto, J. P. H. B., Ehleringer, J. R., Domingues, T. F., Berry, J. A., Ishida, F. Y., Mazzi, E., Higuchi, N., Flanagan, L. B., Nardoto, G. B., and Martinelli, L. A.: The stable carbon and nitrogen isotopic composition of vegetation in tropical forests of the Amazon Basin, Brazil, Biogeochemistry, 79, 251–274, 2006.

Pataki, D. E., Ehleringer, J. R., Flanagan, L. B., Yakir, D., Bowling, D. R., Still, C. J., Buchmann, N., Kaplan, J. O., and Berry, J. A.: The application and interpretation of Keeling plots in terrestrial carbon cycle research, Glob. Biogeochem. Cy., 17(1), 1022, https://doi.org/10.1029/2001gb001850, 2003a.

Pataki, D. E., Ellsworth, D. S., Evans, R. D., Gonzalez-Meler, M., King, J., Leavitt, S. W., Lin, G. H., Matamala, R., Pendall, E., Siegwolf, R., Van Kessel, C., and Ehleringer, J. R.: Tracing changes in ecosystem function under elevated carbon dioxide conditions, Bioscience, 53, 805–818, 2003b.

Pataki, D. E., Lai, C. T., Keeling, C. D., and Ehleringer, J. R.: Insights from stable isotopes on the role of terrestrial ecosystems in the global carbon cycle, in: Terrestrial ecosystems in a changing world, edited by: Canadell, J. G., Pataki, D. E., and Pitelka, L. F., Global change – the IGBP series, Springer, Berlin, Heildelberg, Germany, 37–44, 2007.

Ponton, S., Flanagan, L. B., Alstad, K. P., Johnson, B. G., Morgenstern, K., Kljun, N., Black, T. A., and Barr, A. G.: Comparison of ecosystem water-use efficiency among Douglas-fir forest, aspen forest and grassland using eddy covariance and carbon isotope techniques, Global Change Biology, 12, 294–310, 2006.

Schulze, E. D.: Carbon-dioxide and water-vapor exchange in response to drought in the atmosphere and in the soil, Annual Review of Plant Physiology and Plant Molecular Biology, 37, 247–274, 1986.

Sokal, R. R., and Rohlf, F. J.: Biometry the principles and practice of statistics in biological research, 3 ed., W. H. Freeman and Company, New York, 887 pp., 1995.

Souza, J. S. de: Dinâmica espacial e temporal do fluxo de CO2 do solo em floresta de terra firme na Amazônia Central, M.S. thesis, Coordenação de Ciências Florestais Tropicais, Instituto Nacional de Pesquisas da Amazônia, Universidade Federal do Amazonas, Manaus, Brazil, 62 pp., 2004.

Sparks, J. P. and Ehleringer, J. R.: Leaf carbon isotope discrimination and nitrogen content for riparian trees along elevational transects, Oecologia, 109, 362–367, 1997.

Sternberg, L. D. L., Mulkey, S. S., and Wright, S. J.: Ecological interpretation of leaf carbon isotope ratios: influence of respired carbon dioxide, Ecology, 70, 1317–1324, 1989.

Sternberg, L. D. S., Moreira, M. Z., Martinelli, L. A., Victoria, R. L., Barbosa, E. M., Bonates, L. C. M., and Nepstad, D. C.: Carbon dioxide recycling in two Amazonian tropical forests, Agricultural and Forest Meteorology, 88, 259–268, 1997.

Stewart, G. R., Turnbull, M. H., Schmidt, S., and Erskine, P. D.: $^13$C natural-abundance in plant communities along a rainfall gradient: a biological integrator of water availability, Australian Journal of Plant Physiology, 22, 51–55, 1995.

Tu, K. and Dawson, T.: Partitioning ecosystem respiration using stable carbon isotope analyses of CO2, in: Stable isotopes and biosphere-atmosphere interactions Processes and biological controls, 1st ed., edited by: Flanagan, L. B., Ehleringer, J. R., and Pataki, D. E., Physiological ecology, Elsevier Academic Press, London, UK, 125–153, 2005.

Vandermerwe, N. J., and Medina, E.: Photosynthesis and $^13$C/$^12$C ratios in Amazonian rain forests, Geochimica et Cosmochimica Acta, 53, 1091-1094, 1989.

Vitousek, P. M., Field, C. B., and Matson, P. A.: Variation in foliar $\delta ^13$C in Hawaiian \textitMetrosideros polymorpha: a case of internal resistance?, Oecologia, 84, 362–370, 1990.

Waterloo, M. J., Oliveira, S. M., Drucker, D. P., Nobre, A. D., Cuartas, L. A., Hodnett, M. G., Langedijk, I., Jans, W. W. P., Tomasella, J., de Araujo, A. C., Pimentel, T. P., and Estrada, J. C. M.: Export of organic carbon in run-off from an Amazonian rainforest blackwater catchment, Hydrological Processes, 20, 2581–2597, 2006.

Werner, C., Unger, S., Pereira, J. S., Maia, R., David, T. S., Kurz-Besson, C., David, J. S., and Maguas, C.: Importance of short-term dynamics in carbon isotope ratios of ecosystem respiration ($\delta ^13$C$_R)$ in a Mediterranean oak woodland and linkage to environmental factors, New Phytologist, 172, 330–346, 2006.

White, J. and Vaughn, B.: Stable isotopic composition of atmospheric carbon dioxide ($^13$C and $^18$O) from the NOAA GMD carbon cycle cooperative global air sampling network, 1990–2005, version: 2006-12-01.1456, available at: ftp://ftp.cmdl.noaa.gov/ccg/co2c13/flask/event/, 2007.

Zimmerman, J. K., and Ehleringer, J. R.: Carbon isotope ratios are correlated with irradiance levels in the Panamanian orchid \textitCatasetum viridiflavum, Oecologia, 83, 247–249, 1990.

Zobitz, J. M., Keener, J. P., Schnyder, H., and Bowling, D. R.: Sensitivity analysis and quantification of uncertainty for isotopic mixing relationships in carbon cycle research, Agricultural and Forest Meteorology, 136, 56–75, 2006.